Pone 0280098

PLOS ONE
RESEARCH ARTICLE
Broad-spectrum infrared thermography for

detection of M2 digital dermatitis lesions on
hind feet of standing dairy cattle
Arne Vanhoudt ID1¤a*, Casey Jacobs2¤b, Maaike Caron1¤c, Herman W. Barkema2,
Mirjam Nielen ID1, Tine van Werven1,3, Karin Orsel2
1 Department of Population Health Sciences, Faculty of Veterinary Medicine, Utrecht University, Utrecht,
Utrecht, The Netherlands, 2 Department of Production Animal Health, Faculty of Veterinary Medicine,
University of Calgary, Calgary, Alberta, Canada, 3 University Farm Animal Practice, Utrecht University,
a1111111111 Harmelen, Utrecht, The Netherlands
a1111111111
a1111111111 ¤a Current address: Royal GD, Deventer, Overijssel, The Netherlands
a1111111111 ¤b Current address: More Than Just Feed, Alberta, Canada
a1111111111 ¤c Current address: Vee&Arts Farm Animal Practice, Bergen op Zoom, North Brabant, The Netherlands
* vanhoudt.arne@gmail.com
Abstract
OPEN ACCESS
Low-effort, reliable diagnostics of digital dermatitis (DD) are needed, especially for lesions
Citation: Vanhoudt A, Jacobs C, Caron M, Barkema
HW, Nielen M, van Werven T, et al. (2023) Broad- warranting treatment, regardless of milking system or hygienic condition of the feet. The pri-
spectrum infrared thermography for detection of mary aim of this study was to test the association of infrared thermography (IRT) from
M2 digital dermatitis lesions on hind feet of
unwashed hind feet with painful M2 lesions under farm conditions, with lesion detection as
standing dairy cattle. PLoS ONE 18(1): e0280098.
https://doi.org/10.1371/journal.pone.0280098 ultimate goal. Secondary objectives were to determine the association between IRT from
washed feet and M2 lesions, and between IRT from unwashed and washed feet and the
Editor: Julio Cesar de Souza, Universidade Federal
de Mato Grosso do Sul, BRAZIL presence of any DD lesion. A total of 641 hind feet were given an M-score and IRT images
of the plantar pastern were captured. Multivariable logistic regression analyses were done
Received: April 29, 2022
with DD status as dependent variable and maximum infrared temperature (IRTmax), lower
Accepted: December 20, 2022
leg cleanliness score and locomotion score as independent variables, and farm as fixed
Published: January 17, 2023 effect. To further our understanding of IRTmax within DD status, we divided IRTmax into
Peer Review History: PLOS recognizes the two groups over the median value of IRTmax in the datasets of unwashed and washed feet,
benefits of transparency in the peer review respectively, and repeated the multivariable logistic regression analyses. Higher IRTmax
process; therefore, we enable the publication of
from unwashed hind feet were associated with M2 lesions or DD lesions, in comparison with
all of the content of peer review and author
responses alongside final, published articles. The feet without an M2 lesion or without DD, adjusted odds ratio 1.6 (95% CI 1.2–2.2) and 1.1
editorial history of this article is available here: (95% CI 1.1–1.2), respectively. Washing of the feet resulted in similar associations. Dichoto-
https://doi.org/10.1371/journal.pone.0280098 mization of IRTmax substantially enlarged the 95% CI for the association with feet with M2
Copyright: © 2023 Vanhoudt et al. This is an open lesions indicating that the association becomes less reliable. This makes it unlikely that IRT-
access article distributed under the terms of the max alone can be used for automated detection of feet with an M2 lesion. However, IRTmax
Creative Commons Attribution License, which
can have a role in identifying feet at-risk for compromised foot health that need further exam-
permits unrestricted use, distribution, and
reproduction in any medium, provided the original ination, and could therefore function as a tool aiding in the automated monitoring of foot
author and source are credited. health on dairy herds.
Data Availability Statement: Due to a signed
agreement between the researchers and farmers
we are unable to make all data underlying the
findings of this manuscript fully available without
PLOS ONE | https://doi.org/10.1371/journal.pone.0280098 January 17, 2023 1 / 14

PLOS ONE Infrared thermography for digital dermatitis detection
restriction. Restrictions on this dataset were Introduction

imposed by Cattle Health Research Group,
Department of Production Animal Health, Faculty of Digital dermatitis (DD) is a multifactorial, infectious, polytreponemal disease, characterized
Veterinary Medicine, University of Calgary, Calgary, by ulcerative or hyperkeratotic lesions that are typically located between the heel bulbs of hind
Alberta, Canada. Access to the anonymised dataset feet [1]. It affects dairy cattle worldwide and cattle with DD have reduced animal welfare, pro-
for research involving the research group that duction and reproductive performance, resulting in economic losses and increased labour for
collected the original data is possible, and enquiries
the farmers [2–4].
for this purpose can be made by contacting the
corresponding author or research group Current control of DD relies on keeping the disease in a manageable state [5] and entails
(headpah@ucalgary.ca or karin.orsel@ucalgary. both disease prevention through footbathing at herd level and treatment of ulcerative lesions
ca). at cow level. These ulcerative lesions are commonly grouped as active lesions and consist of
Funding: This study was funded by CAAP the M1, M2, and M4.1 stage lesions [6].
(Canadian Agriculture Adaptation Program; Detection of DD lesions is often late and typically takes place either during routine
Canada; http://omaf.gov.on.ca/english/food/ foot trimming or when cows are seen lame or standing on tiptoes due to a painful lesion.
industry/can-agri-adapt.htm), Alberta Milk Visual inspection of the feet in the trimming chute is considered best practice for the
(Edmonton, Alberta, Canada; https://albertamilk.
diagnosis of DD [7]. However, often this is not practical due to time and labour require-
com/), and DeLaval Manufacturing (Kansas City,
Missouri, United States of America; https://www.
ments and typically is not performed on a routine basis at herd level which is essential for
delaval.com/en-us/) The funders had no role in early detection and treatment of M2 lesions [8]. Prompt effective treatment of M2 lesions
study design, data collection and analysis, decision deals with the welfare aspect of DD, as Higginson Cutler et al. [3] described these lesions
to publish, or preparation of the manuscript. as most painful.
Competing interests: The authors have declared Consequently, scoring feet in the milking parlour after feet have been hosed off with water
that no competing interests exist. was successfully tested as an alternate diagnostic tool, compared to identification in the trim-
ming chute, with a sensitivity (Se) and specificity (Sp) for detecting M2 lesions of about 0.60
and 1.00, respectively [7]. Others compared scoring in the milking parlour with the trimming
chute for presence or absence of a DD lesion, regardless the M-stage, and reported Se 0.55–
1.00 and Sp 0.80–1.00 [8–10]. Due to the absence of a milking parlour on dairy herds with an
automatic milking system, routine screening of DD on these herds must occur during pen
walks or by running the entire herd through the trimming chute. Cramer et al. [8] reported
pen walks to have poor discerning capacity for M-stages of DD.
There is, therefore, an urgent need for a reliable method to quickly and easily diagnose
M2 lesions which is widely applicable regardless the hygienic condition of the feet, nor
dependent of milking system. A small number of studies investigated the use of infrared
thermography (IRT) for the purpose of detecting the presence of DD, regardless the M-
stage. This technology is based on detecting infrared radiation, which is emitted by all
objects, depending on their temperature. Skin temperature is highly dependent on the tem-
perature of the underlying tissue and circulation. Therefore, variations in skin temperature,
captured by an IRT camera, can be related to underlying inflamed tissue or altered meta-
bolic activity [11], as may occur during inflammation caused by DD. In a study by Stokes
et al. [12], maximum infrared temperature (IRTmax) of the plantar pastern was higher on
feet with DD from standing cattle in comparison with feet without any lesions. However,
IRTmax was not different between feet with DD lesions and feet with other lesions [12].
Alsaaod et al. [13] were able to detect hind feet with DD in standing cows using the differ-
ence between IRTmax of hind and front feet.
For practical and technical reasons, M2 detection on unwashed feet is preferred over
detection on pre-washed feet [12]. The primary objective of this study was, therefore, to
determine whether broad spectrum IRT from unwashed hind feet of cows standing in a
milking parlour was associated with M2 lesions. As secondary objectives, we investigated
the association of IRT from pre-washed standing hind feet with M2 lesions and the associa-
tion of IRT from unwashed and washed standing hind feet with the presence of DD, regard-
less of M-score.

Materials and methods

Study design and ethical statement
We analysed data collected in parallel with the published randomized controlled trial by Jacobs
et al. [14]. The IRT measurements and locomotion scores (LS) were not analysed before,
whereas the M-scores, lower leg cleanliness scores (CS), and farm descriptives were used from
Jacobs et al. [14]. All methods were approved by the Animal Care Committee (AC13-0055) of
the University of Calgary. Written informed consent was obtained from the herd owners prior
to participation in the study.
Participating dairy farms met the following criteria: � 60 lactating dairy cows, > 90% Hol-
stein-Friesian cows, lactating cows housed in freestall barns and milked in a parlour. On a con-
venience sample of four farms, a target of 40 dairy cows were semi-randomly selected by
dividing the number of milking cows, as stated by the farmer, by 40 and selecting every nth
cow in the milking parlour. These four farms were visited at 3-week intervals for a total of 12
weeks, resulting in five visits with data collection per farm. An opportunistically selected fifth
farm, was visited once to collect IRT images and M-scores only. On this fifth farm, data was
collected from as many hind feet as possible without delaying the milking routine. This
resulted in data collection from 131 of the 186 cows being milked during the visit. Each farm
was located in Alberta, Canada, and data were collected from May to August 2013 on the first
four farms and in November 2013 on the fifth farm. The routine treatment and hoof trimming
schedule was maintained for all farms over the course of the study [14]. We refer the reader to
Jacobs et al. [14] for details on the footbathing practices for lactating cows. Where farm 1 cor-
responds with farm C4, farm 2 with farm C3, farm 3 with Q3, farm 4 with Q4, and farm 5 with
Q6 in Jacobs et al. [14].
Clinical scores and infrared thermography data collection

One observer (CJ), trained in scoring using digital colour images, videos and definitions,
scored all feet in the study and took all IRT images. During data collection the observer was
aided by one other person to keep records. All data were collected during milking from both
standing hind feet of recruited cows only. First, data were collected from recruited cows on
one side of the parlour, followed by recruited cows on the other side of the parlour. The order
of data collection remained the same throughout the study: CS, IRT image capture of
unwashed feet, wash feet with water using a water source that was available in the parlour, IRT
image capture of washed feet, and M-score washed feet. For the IRT images of washed feet, the
amount of time between washing feet and capturing the second IRT image varied according to
the milking routine and size of the milking parlour. Recruited cows were video recorded while
exiting the milking parlour, and these recordings were used for locomotion scoring.
The CS was done as developed by Cook [15] and adapted by Solano et al. [16] and was
scored from 1 to 4 according to varying contamination: 1 = fresh manure for < 50%; 2 = fresh
manure for > 50%; 3 = dried caked and fresh manure for > 50%; and 4 = entire area with
dried caked manure. Scoring for DD was according to the M-stage classification developed by
Döpfer et al. [17], using a headlamp and a cosmetic mirror glued to a kitchen spatula [7, 9]. In
summary, M0 was defined as normal digital skin with no evidence of DD; M1 was defined as a
small (< 2 cm in diameter) circumscribed red to grey epithelial defect; M2 was defined as an
ulcerative lesion � 2 cm in diameter with a red-grey surface; M3 was defined as a stage charac-
terized by a firm dark scab-like covering; and M4 was characterized by a lesion surface with
brown or black tissue that was hyperkeratotic, scaly, or proliferative. As in Jacobs et al. [14],
the M4.1 lesions, with small red circumscribed lesions occurring within the boundaries of an

existing M4 lesion [18], were not scored as such, and therefore lesions of this description were
included within the M1 category. The LS considered five classes, with 1 = perfect gait and
5 = severely lame, based on the 7 specific gait attributes as described by Flower and Weary [19]
and validated for use on video recordings by Chapinal et al. [20] and Ito et al. [21].
Infrared thermography imaging

Thermal images of all hind feet enrolled in the study were obtained with a FLiR i3 handheld
thermal imaging camera (FLiR Systems Inc.) and analysed using ThermaCAM Researcher
Professional 2.8 SR-2 software (FLiR Systems Inc.). Details on the technical characteristics of
the camera are provided in S1 Table. The software package produced specific information
such as minimum, maximum and mean temperature with standard deviation for whole images
or within a specific area using a geometric figure drawn on the image. Thermal images of the
plantar pastern, focused on the cleft between the heel bulbs, were taken at a distance of approx-
imately 0.5 m. To analyse the IRT images, the rectangle tool of the software was used to select
the plantar aspect of the hind feet from the bottom of the dewclaws to the heel (Fig 1). The pro-
cessing of all IRT images in the software, including the drawing of the rectangles, was done by
one observer (MC). Previous studies identified IRTmax as the most suitable IRT variable for
research on the association between IRT and foot health [12, 22], hence we only used IRTmax
for the analyses in our study. Thermograph resolution was calibrated to ambient temperature
before each collection session using a Reed LM-800 4-in-1 pocket thermo-anemometer,
hygrometer, thermometer and illuminometer (Reed Instruments).
Statistical analyses
Statistical analyses were conducted using RStudio Version 1.3.1093 [23, 24]. Statistical signifi-
cance was declared at p < 0.05. Handling of the collected data for analysis of the different
objectives is detailed in Fig 2.
First, descriptive analyses were done to identify the number of feet with M2 lesions with
IRTmax available after software processing of the IRT images. At the first visit, 21 hind feet
met these requirements in the unwashed and washed condition. Another 15 unwashed and 19
Fig 1. Example of infrared thermography data collection and analysis of images from FLiR i3 handheld camera using ThermaCAM Researcher
Professional 2.8 SR-2 software.
https://doi.org/10.1371/journal.pone.0280098.g001

Fig 2. Study flow diagram for a study testing the association between broad spectrum infrared thermography and
the presence of digital dermatitis lesions using unwashed and washed hind feet from five Canadian dairy herds.
The first four herds were visited at 3-week intervals for a total of 12 weeks, resulting in five visits with data collection
per farm and the fifth farm was visited once. The bold lines represent general study recruitment, the solid lines
represent the unwashed hind feet and the dotted lines represent the washed hind feet. The diagram was created with
www.app.diagrams.net.
washed hind feet were available from the other visits. Because of the low prevalence of M2
lesions in the dataset, it was decided to complement the data from the first visit with M2 scored
feet only from the following visits for further statistical analyses.

Prior to statistical analyses, CS and LS were dichotomized. Dichotomization of the CS was

based on presence of dried manure or not, with CS 1 and 2 categorized as ‘fresh manure’ and
CS 3 and 4 as ‘dried manure’ [25]. Dichotomization of the LS was based on presence of limping
indicating lameness with LS 1 and 2 as ‘not lame’ and LS 3, 4, and 5 as ‘lame’ [26, 27]. Associa-
tions were first assessed using univariable logistic regression analyses between DD status and
IRTmax, CS, LS, and farm, respectively; and second using multivariable logistic regression
analysis. The dependent variable was DD status (M2 = 1 and M0|M1|M3|M4 = 0; or DD pres-
ent = 1 and absent = 0) and independent variables were IRTmax, CS, and LS. Farm was fixed
into the model as a means to account for farm effect and clustering of cows within farm. The
final reduced model was based on the lowest Akaike information criterion using a backward
elimination approach [28]. Univariable logistic regression analyses used both the full categori-
cal and dichotomized CS and LS, and results hereof informed variable selection for the multi-
variable models. To further our understanding of IRTmax within DD status, we divided IRT
max into two groups over the median value of IRTmax, regardless of M-score, in the datasets
of unwashed and washed feet, respectively, and repeated the multivariable logistic regression
analyses as described above. The full results of all regression analyses are reported in the sup-
porting information (S1 File).
Results
A total of 641 hind feet from 310 cows of 5 farms were enrolled in the study (Fig 2). After dis-
carding feet missing an IRTmax value, either due to absence of an IRT image or inability to
process the IRT image with the software, and discarding feet missing an M-score, a total of 529
unwashed hind feet from 285 cows and a total of 558 washed hind feet from 289 cows with an
IRTmax value and an M-score were available for analysis. The unwashed dataset had 54 cows
with one observation, 218 cows with two observations, and 13 cows with three observations
with IRTmax and M-score data, whereas the washed dataset had 32 cows with one observation,
245 cows with two observations, and 12 cows with three observations with IRTmax and M-
score data. From these, 205 unwashed hind feet from 115 cows and 229 washed hind feet from
123 cows also had both LS and CS data available.
Lactating herd size ranged from 166 to 279 cows and farm-level DD prevalence (at least one
hind foot with DD) in enrolled cows ranged from 62 to 85% (mean 72%, standard deviation 9)
at the first visit. An overview of the M-scores by farm, LS, and CS for the hind feet with an IRT-
max in our study is provided in Table 1. The unwashed hind feet dataset contained 36 feet
with an M2 lesion and 493 feet without an M2 lesion, and 310 feet with DD and 219 feet with-
out DD. The washed hind feet dataset contained 40 feet with an M2 lesion and 518 feet without
an M2 lesion, and 329 feet with DD and 229 feet without DD. Table 2 provides an overview of
the descriptive statistics of IRTmax for each group of hind feet and boxplots of the IRTmax are
provided in Fig 3.
Association of maximum infrared temperature with the presence of M2

lesions
In the final multivariable logistic regression analysis models of our study, higher IRTmax val-
ues were associated with an increased odds for M2 lesions on both unwashed (adjusted OR
1.6; 95% CI 1.2–2.2) and washed hind feet (adjusted OR 1.4; 95% CI 1.1–1.7), as was presence
of dried manure on the lower hind legs (CS = 3 and 4; Table 3). These associations remained
similar after dichotomization of IRT max with an adjusted OR of 13.9 (95% CI 3.4–95.7) and
4.8 (95% CI 1.7–15.8) for unwashed and washed hind feet, respectively.

Table 1. M-scores for digital dermatitis, locomotion score, and cleanliness score for hind feet before and after washing from five Canadian dairy herds.
Unwashed hind feet Washed hind feet
M0 M1 M2 M3 M4 Total M0 M1 M2 M3 M4 Total
Herd
1 22 0 2 21 15 60 32 0 3 24 18 77
2 27 1 14 50 21 113 23 1 13 51 20 108
3 36 1 7 13 15 72 36 1 9 15 17 78
4 15 0 1 28 4 48 14 0 3 32 5 54
5 119 2 12 33 70 236 124 2 12 34 69 241
Total 219 4 36 145 125 529 229 4 40 156 129 558
LSb
1 45 1 10 57 20 133 49 1 12 60 23 145
2 10 0 6 20 7 43 11 0 6 19 8 44
3 7 0 0 8 6 21 11 0 2 11 8 32
4 4 0 2 2 0 8 4 0 2 3 0 9
5 0 0 0 0 1 1 0 0 0 0 0 0
Total 66 1 18 87 34 206 75 1 22 93 39 230
CSc
1 10 0 2 8 6 26 6 0 2 10 6 24
2 61 2 7 66 29 165 65 2 6 73 32 178
3 26 0 14 34 20 94 32 0 19 36 22 109
4 3 0 0 4 0 7 2 0 0 3 0 5
Total 100 2 23 112 55 292 105 2 27 122 60 316
a
M-stages [17] were determined in-parlour, after washing the feet with water. The M4.1 stage by Berry et al. [18] is included in the M1 stage.
b
Locomotion scores [19] were determined from video recordings of cows exiting the milking parlour with score � 3 considered lame; only available for feet from farm
1 to 4.
c
Lower leg cleanliness scores [15, 16] were determined in-parlour with presence of dried manure in score � 3; only available for feet from farm 1 to 4.
https://doi.org/10.1371/journal.pone.0280098.t001
Association of maximum infrared temperature with the presence of digital

dermatitis lesions
Multivariable logistic regression analyses identified that higher IRTmax values were associated
with an increased odds for DD presence on both unwashed (adjusted OR 1.1; 95% CI 1.1–1.2)
Table 2. Descriptive statistics for maximum infrared temperature (˚C) of the plantar pastern from standing dairy cattle feet before and after washing, categorized
by digital dermatitis (DD) status.
DD status N mean SD minimum Q1 median Q3 maximum
Unwashed hind feet
M2a 36 32.1 1.2 28.8 31.5 32.2 33.0 34.3
M0|M1|M3|M4a 493 30.3 2.8 18.4 29.0 30.7 32.2 35.4
DD present 310 30.9 2.4 20.3 29.7 31.2 32.5 35.4
DD absent 219 29.7 3.1 18.4 28.1 30.3 31.9 34.4
Washed hind feet
M2a 40 32.1 1.3 29.0 31.3 32.3 32.9 34.7
M0|M1|M3|M4a 518 30.5 3.0 17.3 29.3 31.2 32.5 35.3
DD present 329 31.1 2.4 19.0 29.8 31.5 32.8 35.3
DD absent 229 29.9 3.4 17.3 28.4 31.0 32.4 35.1
a
M-stages [17] were determined in-parlour, after washing the feet with water; the M4.1 stage by Berry et al. [18] is included in the M1 stage.

Fig 3. Boxplots for maximum infrared temperature (IRTmax) from the pastern region of dairy cattle hind feet
before and after washing. (A) For hind feet with M2 or M0|M1|M3|M4 lesions of digital dermatitis (DD). (B) For
hind feet with absence or presence of DD. Bold solid line = median, box = interquartile range (IQR), bottom
whisker = 25th percentile—1.5 x IQR, top whisker = 75th percentile + 1.5 x IQR, circle = datapoint outside the
interwhisker range.
and washed hind feet (adjusted OR 1.1; 95% CI 1.1–1.2; Table 4). This association disappeared
after dichotomization of IRTmax.
Discussion
This multi-farm study provides insights into the practical application of IRT for detection of
DD, M2 lesions in particular, on hind feet from standing cows with a handheld IRT camera.
Higher IRTmax values were associated with feet with M2 lesions or DD lesions, in comparison
with feet without an M2 lesion or without DD, respectively, regardless of the hygienic condi-
tion of the feet. Dichotomization of IRTmax substantially enlarged the 95% CI for the associa-
tion with feet with M2 lesions indicating that the association becomes less reliable. When
looking at feet with any DD lesions, there was no association with the dichotomized IRTmax.
Previous work reported poor test characteristics to diagnose the presence of DD lesions using
IRTmax with Se 0.75–0.89 and Sp 0.65–0.70 [13, 29]. Altogether, these findings suggest that it
is unlikely that a cut-off value for IRTmax with high Se and Sp for the detection of feet with
M2 lesions can be determined using cross-sectional data.

Table 3. Final reduced multivariable logistic regression models to test the association between maximum infrared temperature (IRTmax) from the plantar pastern
and presence of M2 lesions [17] of digital dermatitis on hind feet from standing dairy cattle before and after washing, with lower leg cleanliness score (CS) [15, 16]
as explanatory variable and farm as fixed effect.
Model Variable Adjusted OR 95% CI
Unwashed hind feet
Continuous IRTmax
IRTmax + CS + farm IRTmax 1.6 1.2–2.2
CS fresh manure 1 referent
CS dried manure 4.1 1.6–10.7
Farm 1 1 referent
Farm 2 2.1 0.5–14.2
Farm 3 5.5 1.2–40.5
Farm 4 0.4 0.1–4.9
Dichotomized IRTmaxa
IRTmax + CS + farm IRTmax < 31.0˚C 1 referent
IRTmax � 31.0˚C 13.9 3.4–95.7
Farm 1 1 referent
Farm 2 2.2 0.5–15.2
Farm 3 6.4 1.3–48.7
Farm 4 0.5 0.1–5.6
Washed hind feet
Continuous IRTmax
IRTmax + CS + farm IRTmax 1.4 1.1–1.7
Farm 1 1 referent
Farm 2 3.9 1.1–17.9
Farm 3 10.7 2.7–56.0
Farm 4 1.9 0.3–11.4
IRTmax + CS + farm IRTmax < 31.3˚C 1 referent
IRTmax � 31.3˚C 4.8 1.7–15.8
Farm 1 1 referent
Farm 2 4.0 1.2–18.5
Farm 3 9.4 2.4–48.4
Farm 4 2.0 0.3–11.4
a
IRTmax was divided into 2 groups over the median value of IRTmax, regardless of M-score [17], in the datasets of unwashed and washed feet, respectively.
In analogy with machine learning techniques used for automated mastitis or oestrus detec-
tion [30, 31], similar techniques can be developed to use IRTmax for the detection of M2
lesions in which the IRTmax from a foot is compared with rolling averages of the same foot,
contralateral foot, feet average within cow, herd average, or a combination of these. To date,
the authors are unaware of publications that report investigations of this option.
A limitation of this study was the low prevalence of feet with M2 lesions and of lame feet.
Although this is a realistic reflection of the average Canadian dairy herd [27, 32], it resulted

Table 4. Final reduced multivariable logistic regression analyses to test the association between maximum infrared temperature (IRTmax) from the plantar pastern
and presence of any lesions of digital dermatitis on hind feet from standing dairy cattle before and after washing, with farm as fixed effect.
Model Variable Adjusted OR 95% CI
Unwashed hind feet
Continuous IRTmax
IRTmax + farm IRTmax 1.1 1.1–1.2
Farm 1 1 referent
Farm 2 1.4 0.7–2.8
Farm 3 0.7 0.3–1.4
Farm 4 1.2 0.6–2.8
Farm 5 0.6 0.3–0.9
IRTmax + farm IRTmax < 31.0˚C 1 referent
IRTmax � 31.0˚C 1.4 0.9–2.1
Farm 1 1 referent
Farm 2 1.6 0.8–3.2
Farm 3 0.6 0.3–1.2
Farm 4 1.3 0.6–2.9
Farm 5 0.6 0.3–0.9
Washed hind feet
Continuous IRTmax
IRTmax + farm IRTmax 1.1 1.1–1.2
Farm 1 1 referent
Farm 2 2.7 1.4–5.2
Farm 3 1.3 0.7–2.7
Farm 4 2.4 1.1–5.4
Farm 5 0.8 0.5–1.4
IRTmax + farm IRTmax < 31.3˚C 1 referent
IRTmax � 31.3˚C 1.2 0.8–1.7
Farm 1 1 referent
Farm 2 2.6 1.4–5.1
Farm 3 0.9 0.5–1.7
Farm 4 2.1 1.0–4.7
Farm 5 0.7 0.4–1.2
a
IRTmax was divided into two groups over the median value of IRT max, regardless of M-score [17], in the datasets of unwashed and washed feet, respectively.
in a statistically unbalanced dataset. It is possible that this restricted the capacity of our
study to detect an association with IRTmax. Also, our dataset contained a large number of
animals with only one observation, making the inclusion of cow as a random effect, to
account for repeated measures and cows having more than one observation, in our models
impossible.
The M-score of the feet in this study was determined by visual inspection of the feet in
the milking parlour. Although visual detection of M-scores in the milking parlour versus
in the trimming chute was validated [7], we hereby compared IRTmax with an imperfect
diagnostic test. Potentially, IRTmax could have correctly diagnosed some feet with M2
lesions that were misclassified as feet without M2 lesions by the in-parlour M-scoring
due to the limited Se (0.62) of in-parlour M-scoring for M2 lesions [7]. Diagnosis of DD

in the trimming chute would have reduced possible misclassification of M-scores. Addi-
tionally, information on the presence of other foot lesions, such as claw horn lesions,
could have been collected as feet with other foot lesions typically tend to have higher
IRTmax values compared to feet with no lesions [12, 33–35]. However, inspection of feet
in a trimming chute would have neglected the need for an easy, practical method. Higher
IRTmax values from cattle feet have also been associated with higher ambient tempera-
tures [33, 34], stage of lactation � 200 DIM [33], and more recently with higher locomo-
tion scores in a herd without DD [36]. Some of these factors will have been captured by
fixing farm into the models, but it is likely that they exert an unmeasured effect on the
results of our study.
Further research should aim to include all above-mentioned factors with a preference for
longitudinal studies to better evaluate IRT as an early detection method for M2 lesions result-
ing in lameness. However, these multiple factors which influence the ability to detect M2
lesions, and foot lesions in general, all need to be automatically measured and considered
before IRT can be easily used as a detection tool on farm. Until this further research is done,
the main potential use of IRT in automated detection of foot health status is likely limited to
identify ‘feet at risk’ that need further attention. At-risk feet could either be visually appraised
in the trimming chute, or by computer vision and machine learning technology. The YOLOv2
computer vision model of Cernek et al. [37] correctly classified about 60% of the lesions as an
M2 lesion on washed hind feet in an external validation trial on a commercial US dairy herd.
Combining IRT with other automated lameness detection devices presumably aids in the iden-
tification of feet at risk of compromised foot health.
Conclusions
The presence of M2 lesions on hind feet was associated with higher IRTmax values of the plan-
tar pastern, both on unwashed and washed feet from standing dairy cattle. Dichotomization of
IRTmax substantially decreased the reliability of this association, making it unlikely that IRT-
max alone can be used for automated detection of feet with an M2 lesion. It is probable that
IRTmax does have a role in identifying feet at-risk for compromised foot health that need fur-
ther checking and thereby is a tool that can aid in the automation of monitoring the foot health
status on dairy herds.
Supporting information
S1 Table. Technical data for the FLiR i3 handheld infrared thermography camera.
(DOCX)
S1 File. Regression analyses M2 lesions. Full results of all regression analyses performed
investigating the association between maximum infrared temperature (IRTmax) of the plantar
pastern region of feet from standing dairy cattle and the presence of M2 lesions of digital der-
matitis.
(DOCX)
S2 File. Regression analyses digital dermatitis lesions. Full results of all regression analyses
performed investigating the association between maximum infrared temperature (IRTmax) of
the plantar pastern region of feet from standing dairy cattle and the presence of any lesions of
digital dermatitis.
(DOCX)

Acknowledgments
The authors thank participating farmers for their willingness, time, and cooperation on this
project. Additional thanks to Kelsey Gray and Gwen Roy (University of Calgary, Alberta, Can-
ada) for assistance with data collection. Special thank you to Al Schaefer and Pierre Lepage
(Lacombe Research and Development Centre, Alberta, Canada) for assistance and guidance
regarding the use of IRT cameras. The authors are also grateful for the advice of Hans Vernooij
(Utrecht University, Utrecht, the Netherlands) on the statistical analyses and the help of
Lisanne van der Voort (Utrecht University, Utrecht, the Netherlands) for preparing the
figures.
Author Contributions
Conceptualization: Arne Vanhoudt, Casey Jacobs, Herman W. Barkema, Mirjam Nielen,
Tine van Werven, Karin Orsel.
Data curation: Casey Jacobs, Maaike Caron.
Formal analysis: Arne Vanhoudt, Casey Jacobs, Maaike Caron.
Funding acquisition: Casey Jacobs, Herman W. Barkema, Karin Orsel.
Investigation: Arne Vanhoudt, Casey Jacobs, Maaike Caron, Mirjam Nielen,
Tine van Werven, Karin Orsel.
Methodology: Arne Vanhoudt, Casey Jacobs, Mirjam Nielen, Tine van Werven, Karin Orsel.
Project administration: Casey Jacobs, Karin Orsel.
Resources: Casey Jacobs, Herman W. Barkema, Mirjam Nielen, Tine van Werven,
Karin Orsel.
Software: Arne Vanhoudt, Casey Jacobs, Maaike Caron.
Supervision: Casey Jacobs, Herman W. Barkema, Mirjam Nielen, Tine van Werven,
Karin Orsel.
Validation: Arne Vanhoudt, Casey Jacobs, Herman W. Barkema, Mirjam Nielen, Tine van
Werven, Karin Orsel.
Visualization: Arne Vanhoudt, Casey Jacobs, Maaike Caron.
Writing – original draft: Arne Vanhoudt, Casey Jacobs, Maaike Caron.
Writing – review & editing: Casey Jacobs, Herman W. Barkema, Mirjam Nielen, Tine van
Werven, Karin Orsel.
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PLOS ONE

Broad-spectrum infrared thermography for

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restriction. Restrictions on this dataset were Introduction

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Materials and methods

Clinical scores and infrared thermography data collection

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Infrared thermography imaging

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Association of maximum infrared temperature with the presence of M2

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Association of maximum infrared temperature with the presence of digital

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